APOBEC affects tumor evolution and age at onset of lung cancer in smokers

T Tongwu Zhang J Jian Sang P Phuc H. Hoang W Wei Zhao J Jennifer Rosenbaum K Kofi Ennu Johnson L Leszek J. Klimczak J John McElderry A Alyssa Klein C Christopher Wirth E Erik N. Bergstrom M Marcos Díaz-Gay R Raviteja Vangara F Frank Colon-Matos A Amy Hutchinson S Scott M. Lawrence N Nathan Cole B Bin Zhu T Teresa M. Przytycka J Jianxin Shi N Neil E. Caporaso R Robert Homer A Angela C. Pesatori D Dario Consonni M Marcin Imielinski S Stephen J. Chanock D David C. Wedge D Dmitry A. Gordenin L Ludmil B. Alexandrov R Reuben S. Harris M Maria Teresa Landi

Abstract

Abstract Most solid tumors harbor somatic mutations attributed to off-target activities of APOBEC3A (A3A) and/or APOBEC3B (A3B). However, how APOBEC3A/B enzymes affect tumor evolution in the presence of exogenous mutagenic processes is largely unknown. Here, multi-omics profiling of 309 lung cancers from smokers identifies two subtypes defined by low (LAS) and high (HAS) APOBEC mutagenesis. LAS are enriched for A3B-like mutagenesis and KRAS mutations; HAS for A3A-like mutagenesis and TP53 mutations. Compared to LAS, HAS have older age at onset and high proportions of newly generated progenitor-like cells likely due to the combined tobacco smoking- and APOBEC3A-associated DNA damage and apoptosis. Consistently, HAS exhibit high expression of pulmonary healing signaling pathway, stemness markers, distal cell-of-origin, more neoantigens, slower clonal expansion, but no smoking-associated genomic/epigenomic changes. With validation in 184 lung tumor samples, these findings show how heterogeneity in mutational burden across co-occurring mutational processes and cell types contributes to tumor development.

Article Details

Volume / Issue Vol. 16, Issue 1
Published May 21, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (31)

T

Tongwu Zhang

J

Jian Sang

P

Phuc H. Hoang

W

Wei Zhao

J

Jennifer Rosenbaum

K

Kofi Ennu Johnson

L

Leszek J. Klimczak

J

John McElderry

A

Alyssa Klein

C

Christopher Wirth

E

Erik N. Bergstrom

M

Marcos Díaz-Gay

R

Raviteja Vangara

F

Frank Colon-Matos

A

Amy Hutchinson

S

Scott M. Lawrence

N

Nathan Cole

B

Bin Zhu

T

Teresa M. Przytycka

J

Jianxin Shi

N

Neil E. Caporaso

R

Robert Homer

A

Angela C. Pesatori

D

Dario Consonni

M

Marcin Imielinski

S

Stephen J. Chanock

D

David C. Wedge

D

Dmitry A. Gordenin

L

Ludmil B. Alexandrov

R

Reuben S. Harris

M

Maria Teresa Landi